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Palliative Effect of Combined Application of Zinc and Selenium on Reproductive Injury Induced by Tripterygium Glycosides in Male Rats

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Abstract

The long-term use of tripterygium glycosides (TG) can lead to male reproductive damage. Research indicates that zinc and selenium exhibit a synergistic effect in the male reproductive system, with the combined preparation demonstrating superior therapeutic effects compared to individual preparations. The purpose of this study was to explore the specific mechanism by which zinc and selenium mitigate reproductive toxicity induced by TG in male rats. Rats were randomly assigned to three groups: control group (C group), model group (M group, receiving TG at 30 mg/kg/day), and model + zinc + selenium group (ZS group). The ZS group was also given TG gavage for the first 4 weeks. Starting from the fifth week until the conclusion of the eighth week, the ZS group received an additional protective treatment of 10 mg/kg/day Zn and 0.1 mg/kg/day Se 4 h after TG administration. Following euthanasia, blood samples, rat testis, and epididymis tissues were collected for further experiments. Combined zinc-selenium treatment corrects the imbalance of zinc-selenium homeostasis in testicular tissue induced by TG. This is achieved by upregulating the expression of metal transcription factor (MTF1) and zinc transporters ZIP8 and ZIP14 and downregulating the expression of ZnT10. Improvement of zinc and selenium homeostasis enhanced the expression of zinc-containing enzymes (ADH, LDH, and ALP) and selenoproteins (GPx1 and SELENOP) in the testis. At the same time, zinc and selenium mitigate TG-induced reproductive damage by promoting the activity of antioxidant enzymes and upregulating the expression of proteins associated with the oxidative stress pathway, including Nrf2, Keap1, HO-1, PI3K, and p-AKT.

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Data Availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Ding Q, Wu Y, Liu W (2021) Molecular mechanism of reproductive toxicity induced by Tripterygium wilfordii based on network pharmacology. Medicine (Baltimore) 100(27):e26197. https://doi.org/10.1097/md.0000000000026197

    Article  CAS  PubMed  Google Scholar 

  2. Cheng Y, Chen G, Wang L, Kong J, Pan J, Xi Y, Shen F, Huang Z (2018) Triptolide-induced mitochondrial damage dysregulates fatty acid metabolism in mouse sertoli cells. Toxicol Lett 292:136–150. https://doi.org/10.1016/j.toxlet.2018.04.035

    Article  CAS  PubMed  Google Scholar 

  3. Guo J, Huang Y, Lei X, Zhang H, Xiao B, Han Z, Liang C, Yang W (2019) Reproductive systemic toxicity and mechanism of glucosides of Tripterygium wilfordii Hook. F. (GTW). Ann Clin Lab Sci 49(1):36–49

    CAS  PubMed  Google Scholar 

  4. Chang Z, Qin W, Zheng H, Schegg K, Han L, Liu X, Wang Y, Wang Z, McSwiggin H, Peng H, Yuan S, Wu J, Wang Y, Zhu S, Jiang Y, Nie H, Tang Y, Zhou Y, Hitchcock MJM et al (2021) Triptonide is a reversible non-hormonal male contraceptive agent in mice and non-human primates. Nat Commun 12(1):1253. https://doi.org/10.1038/s41467-021-21517-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Jiao W, Sun J, Zhang X, An Q, Fu L, Xu W, Xie H, Tang X, Liu J, Hu W, Gu Y, Zhang K (2021) Improvement of Qilin pills on male reproductive function in tripterygium glycoside-induced oligoasthenospermia in rats. Andrologia 53(4):e13923. https://doi.org/10.1111/and.13923

    Article  CAS  PubMed  Google Scholar 

  6. Zhang K, Ge Z, Fu L, An Q, Zhou F, Guo Y, Wang X, Lu W, Liang X, Wang S, Shang X, Gu Y (2018) Qilin pills alleviate oligoasthenospermia by inhibiting Bax-caspase-9 apoptosis pathway in the testes of model rats. Oncotarget 9(31):21770–21782. https://doi.org/10.18632/oncotarget.24985

    Article  PubMed  PubMed Central  Google Scholar 

  7. Maret W (2019) The redox biology of redox-inert zinc ions. Free Radic Biol Med 134:311–326. https://doi.org/10.1016/j.freeradbiomed.2019.01.006

    Article  CAS  PubMed  Google Scholar 

  8. Xue W, Tang Q, Yang L (2022) The combination of ginger and zinc supplement could improve lead-induced reproductive dysfunction by inhibiting apoptosis mediated by oxidative damage and inflammation. Andrologia:e14577. https://doi.org/10.1111/and.14577

  9. Ahsan U, Kamran Z, Raza I, Ahmad S, Babar W, Riaz MH, Iqbal Z (2014) Role of selenium in male reproduction - a review. Anim Reprod Sci 146(1-2):55–62. https://doi.org/10.1016/j.anireprosci.2014.01.009

    Article  CAS  Google Scholar 

  10. Mistry HD, Broughton Pipkin F, Redman CW, Poston L (2012) Selenium in reproductive health. Am J Obstet Gynecol 206(1):21–30. https://doi.org/10.1016/j.ajog.2011.07.034

    Article  CAS  PubMed  Google Scholar 

  11. Kaur S, Saluja M, Aniqa A, Sadwal S (2021) Selenium attenuates bisphenol A incurred damage and apoptosis in mice testes by regulating mitogen-activated protein kinase signalling. Andrologia 53(3):e13975. https://doi.org/10.1111/and.13975

    Article  CAS  PubMed  Google Scholar 

  12. Türk S, Mändar R, Mahlapuu R, Viitak A, Punab M, Kullisaar T (2014) Male infertility: decreased levels of selenium, zinc and antioxidants. J Trace Elem Med Biol 28(2):179–185. https://doi.org/10.1016/j.jtemb.2013.12.005

    Article  CAS  PubMed  Google Scholar 

  13. Chyra-Jach D, Kaletka Z, Dobrakowski M, Machoń-Grecka A, Kasperczyk S, Bellanti F, Birkner E, Kasperczyk A (2020) Levels of macro- and trace elements and select cytokines in the semen of infertile men. Biol Trace Elem Res 197(2):431–439. https://doi.org/10.1007/s12011-019-02022-9

    Article  CAS  PubMed  Google Scholar 

  14. Sun Bo MJ, Peipei D, Zhuaisheng C, Shusong W (2022) Correlation between seminal plasma selenium and serum reproductive hormones, seminal plasma biochemical and oxidative stress levels in infertile men*. Chinese. J Androl 36(2). https://doi.org/10.3969/j.issn.1008-0848.2022.02.009

  15. Sahu C, Dwivedi DK, Jena GB (2020) Zinc and selenium combination treatment protected diabetes-induced testicular and epididymal damage in rat. Hum Exp Toxicol 39(9):1235–1256. https://doi.org/10.1177/0960327120914963

    Article  CAS  PubMed  Google Scholar 

  16. Naderi M, Ahangar N, Badakhshan F, Ghasemi M, Shaki F (2021) Zinc and selenium supplement mitigated valproic acid-induced testis toxicity by modulating the oxidative redox balance in male rats. Anat Cell Biol 54(3):387–394. https://doi.org/10.5115/acb.20.280

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ma J, Tan H, Bi J, Sun B, Zhen Y, Lian W, Wang S (2023) Zinc ameliorates tripterygium glycosides-induced reproductive impairment in male rats by regulating zinc homeostasis and expression of oxidative stress-related genes. Biol Trace Elem Res. https://doi.org/10.1007/s12011-023-03815-9

  18. Maremanda KP, Khan S, Jena GB (2016) Role of zinc supplementation in testicular and epididymal damages in diabetic rat: involvement of Nrf2, SOD1, and GPX5. Biol Trace Elem Res 173(2):452–464. https://doi.org/10.1007/s12011-016-0674-7

    Article  CAS  PubMed  Google Scholar 

  19. Zhang Z, Cheng Q, Liu Y, Peng C, Wang Z, Ma H, Liu D, Wang L, Wang C (2022) Zinc-enriched yeast may improve spermatogenesis by regulating steroid production and antioxidant levels in mice. Biol Trace Elem Res 200(8):3712–3722. https://doi.org/10.1007/s12011-021-02970-1

    Article  CAS  PubMed  Google Scholar 

  20. Santos HO, Teixeira FJ (2020) Use of medicinal doses of zinc as a safe and efficient coadjutant in the treatment of male hypogonadism. Aging Male 23(5):669–678. https://doi.org/10.1080/13685538.2019.1573220

    Article  CAS  PubMed  Google Scholar 

  21. Chen XW, Chu JH, Li LX, Gao PC, Wang ZY, Fan RF (2022) Protective mechanism of selenium on mercuric chloride-induced testis injury in chicken via p38 MAPK/ATF2/iNOS signaling pathway. Theriogenology 187:188–194. https://doi.org/10.1016/j.theriogenology.2022.05.007

    Article  CAS  PubMed  Google Scholar 

  22. Sharma P, Kaur P, Ghanghas P, Kaur J, Kaushal N (2020) Selenium ameliorates ibuprofen induced testicular toxicity by redox regulation: Running head: Se protects against NSAID induced testicular toxicity. Reprod Toxicol 96:349–358. https://doi.org/10.1016/j.reprotox.2020.08.005

    Article  CAS  PubMed  Google Scholar 

  23. Saïd L, Banni M, Kerkeni A, Saïd K, Messaoudi I (2010) Influence of combined treatment with zinc and selenium on cadmium induced testicular pathophysiology in rat. Food Chem Toxicol 48(10):2759–2765. https://doi.org/10.1016/j.fct.2010.07.003

    Article  CAS  PubMed  Google Scholar 

  24. Akintunde JK, Ajiboye JA, Siemuri EO, Olabisi OO (2021) Fansidar drug induces cytotoxicity in some vital tissues in a rat model: combination defensive effect of selenium and zinc capsules. Ther Adv Drug Saf 12:20420986211027101. https://doi.org/10.1177/20420986211027101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hasani M, Saidpour A, Irandoost P, Golab F, Khazdouz M, Qorbani M, Agh F, Mohammad Sharifi A, Vafa M (2021) Beneficial effects of Se/Zn co-supplementation on body weight and adipose tissue inflammation in high-fat diet-induced obese rats. Food Sci Nutr 9(7):3414–3425. https://doi.org/10.1002/fsn3.2203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Fedala A, Adjroud O, Abid-Essefi S, Timoumi R (2021) Protective effects of selenium and zinc against potassium dichromate-induced thyroid disruption, oxidative stress, and DNA damage in pregnant Wistar rats. Environ Sci Pollut Res Int 28(18):22563–22576. https://doi.org/10.1007/s11356-020-12268-9

    Article  CAS  PubMed  Google Scholar 

  27. Lu J, Ji W, Zhao M, Wang M, Yan W, Chen M, Ren S, Yuan B, Wang B, Chen L (2016) Protamine zinc insulin combined with sodium selenite improves glycometabolism in the diabetic KKAy mice. Sci Rep 6:26563. https://doi.org/10.1038/srep26563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Le G, Yang L, Du H, Hou L, Ge L, Sylia A, Muhmood A, Chen X, Han B, Huang K (2022) Combination of zinc and selenium alleviates ochratoxin A-induced fibrosis via blocking ROS-dependent autophagy in HK-2 cells. J Trace Elem Med Biol 69:126881. https://doi.org/10.1016/j.jtemb.2021.126881

    Article  CAS  Google Scholar 

  29. Tariba B, Živković T, Gajski G, Gerić M, Gluščić V, Garaj-Vrhovac V, Peraica M, Pizent A (2017) In vitro effects of simultaneous exposure to platinum and cadmium on the activity of antioxidant enzymes and DNA damage and potential protective effects of selenium and zinc. Drug Chem Toxicol 40(2):228–234. https://doi.org/10.1080/01480545.2016.1199564

    Article  CAS  PubMed  Google Scholar 

  30. Wu DL, Wang TS, Zhang W, Wang JS, Peng DY, Kong LY (2021) NMR-based metabolomics approach to study the effects of Wu-Zi-Yan-Zong-Wan on triptolide-induced oligospermia in rats. J Ethnopharmacol 265:113192. https://doi.org/10.1016/j.jep.2020.113192

    Article  CAS  PubMed  Google Scholar 

  31. Organization WH: Laboratory manual for the examination of human semen and sperm-cervical mucus intraction. https://fctc.who.int/publications/i/item/9789241547789 (2010). Accessed.

  32. Vandecasteele C, Vanhoe H, Dams R, Versieck J (1990) Determination of trace elements in human serum by inductively coupled plasma-mass spectrometry. Biol Trace Elem Res 26(1):553–560. https://doi.org/10.1007/BF02992711

    Article  PubMed  Google Scholar 

  33. Dams R (1994) RNAA as compared to ICP-MS for the analysis of normal human serum. Biol Trace Elem Res 43-45:539–548. https://doi.org/10.1007/bf02917357

    Article  CAS  PubMed  Google Scholar 

  34. Wang J, Miao M, Zhang Y, Liu R, Li X, Cui Y, Qu L (2015) Quercetin ameliorates liver injury induced with Tripterygium glycosides by reducing oxidative stress and inflammation. Can J Physiol Pharmacol 93(6):427–433. https://doi.org/10.1139/cjpp-2015-0038

    Article  CAS  PubMed  Google Scholar 

  35. Dai Y, Sun L, Han S, Xu S, Wang L, Ding Y (2022) Proteomic study on the reproductive toxicity of tripterygium glycosides in rats. Front Pharmacol 13:888968. https://doi.org/10.3389/fphar.2022.888968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wang K, Hu H, Cui W, Zhang X, Tang Q, Liu N, Lan X, Pan C (2021) Palliative effects of metformin on testicular damage induced by triptolide in male rats. Ecotoxicol Environ Saf 222:112536. https://doi.org/10.1016/j.ecoenv.2021.112536

    Article  CAS  PubMed  Google Scholar 

  37. Yamauchi M, Potter JJ, Mezey E (1988) Detection and localization of immunoreactive alcohol dehydrogenase protein in the rat testis. Alcohol-Clin Exp Res 12(1):143–146. https://doi.org/10.1111/j.1530-0277.1988.tb00148.x

    Article  CAS  PubMed  Google Scholar 

  38. Long M, Yang S, Dong S, Chen X, Zhang Y, He J (2017) Characterization of semen quality, testicular marker enzyme activities and gene expression changes in the blood testis barrier of Kunming mice following acute exposure to zearalenone. Environ Sci Pollut Res Int 24(35):27235–27243. https://doi.org/10.1007/s11356-017-0299-1

    Article  CAS  PubMed  Google Scholar 

  39. Bucci D, Isani G, Giaretta E, Spinaci M, Tamanini C, Ferlizza E, Galeati G (2014) Alkaline phosphatase in boar sperm function. Andrology 2(1):100–106. https://doi.org/10.1111/j.2047-2927.2013.00159.x

    Article  CAS  PubMed  Google Scholar 

  40. Corkins ME, May M, Ehrensberger KM, Hu YM, Liu YH, Bloor SD, Jenkins B, Runge KW, Bird AJ (2013) Zinc finger protein Loz1 is required for zinc-responsive regulation of gene expression in fission yeast. Proc Natl Acad Sci U S A 110(38):15371–15376. https://doi.org/10.1073/pnas.1300853110

    Article  PubMed  PubMed Central  Google Scholar 

  41. Du L, Zhang H, Zhao H, Cheng X, Qin J, Teng T, Yang Q, Xu Z (2019) The critical role of the zinc transporter Zip2 (SLC39A2) in ischemia/reperfusion injury in mouse hearts. J Mol Cell Cardiol 132:136–145. https://doi.org/10.1016/j.yjmcc.2019.05.011

    Article  CAS  PubMed  Google Scholar 

  42. Sun B, Ma J, Te L, Zuo X, Liu J, Li Y, Bi J, Wang S (2023) Zinc-deficient diet causes imbalance in zinc homeostasis and impaired autophagy and impairs semen quality in mice. Biol Trace Elem Res 201(5):2396–2406. https://doi.org/10.1007/s12011-022-03324-1

    Article  CAS  Google Scholar 

  43. Qazi IH, Angel C, Yang H, Zoidis E, Pan B, Wu Z, Ming Z, Zeng CJ, Meng Q, Han H, Zhou G (2019) Role of selenium and selenoproteins in male reproductive function: a review of past and present evidences. Antioxidants 8(8). https://doi.org/10.3390/antiox8080268

  44. Ojeda ML, Nogales F, Membrilla A, Carreras O (2019) Maternal selenium status is profoundly involved in metabolic fetal programming by modulating insulin resistance, oxidative balance and energy homeostasis. Eur J Nutr 58(8):3171–3181. https://doi.org/10.1007/s00394-018-1861-4

    Article  CAS  PubMed  Google Scholar 

  45. Sunuwar L, Frkatović A, Sharapov S, Wang Q, Neu HM, Wu X, Haritunians T, Wan F, Michel S, Wu S, Donowitz M, McGovern D, Lauc G, Sears C, Melia J (2020) Pleiotropic ZIP8 A391T implicates abnormal manganese homeostasis in complex human disease. JCI insight 5(20). https://doi.org/10.1172/jci.insight.140978

  46. Zang ZS, Xu YM, Lau ATY (2016) Molecular and pathophysiological aspects of metal ion uptake by the zinc transporter ZIP8 (SLC39A8). Toxicol Res 5(4):987–1002. https://doi.org/10.1039/c5tx00424a

    Article  CAS  Google Scholar 

  47. Liu MJ, Bao S, Gálvez-Peralta M, Pyle CJ, Rudawsky AC, Pavlovicz RE, Killilea DW, Li C, Nebert DW, Wewers MD, Knoell DL (2013) ZIP8 regulates host defense through zinc-mediated inhibition of NF-κB. Cell Rep 3(2):386–400. https://doi.org/10.1016/j.celrep.2013.01.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. McDermott JR, Geng X, Jiang L, Gálvez-Peralta M, Chen F, Nebert DW, Liu Z (2016) Zinc- and bicarbonate-dependent ZIP8 transporter mediates selenite uptake. Oncotarget 7(23):35327–35340. https://doi.org/10.18632/oncotarget.9205

    Article  PubMed  PubMed Central  Google Scholar 

  49. Jenkitkasemwong S, Wang CY, Mackenzie B, Knutson MD (2012) Physiologic implications of metal-ion transport by ZIP14 and ZIP8. Biometals 25(4):643–655. https://doi.org/10.1007/s10534-012-9526-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Downey AM, Hales BF, Robaire B (2016) Zinc transport differs in rat spermatogenic cell types and is affected by treatment with cyclophosphamide. Biol Reprod 95(1):22. https://doi.org/10.1095/biolreprod.116.140558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bosomworth HJ, Thornton JK, Coneyworth LJ, Ford D, Valentine RA (2012) Efflux function, tissue-specific expression and intracellular trafficking of the Zn transporter ZnT10 indicate roles in adult Zn homeostasis. Metallomics 4(8):771–779. https://doi.org/10.1039/c2mt20088k

    Article  CAS  PubMed  Google Scholar 

  52. Bi SS, Talukder M, Jin HT, Lv MW, Ge J, Zhang C, Li JL (2022) Nano-selenium alleviates cadmium-induced cerebellar injury by activating metal regulatory transcription factor 1 mediated metal response. Anim Nutr 11:402–412. https://doi.org/10.1016/j.aninu.2022.06.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Dong G, Chen H, Qi M, Dou Y, Wang Q (2015) Balance between metallothionein and metal response element binding transcription factor 1 is mediated by zinc ions (review). Mol Med Rep 11(3):1582–1586. https://doi.org/10.3892/mmr.2014.2969

    Article  CAS  PubMed  Google Scholar 

  54. Grzywacz A, Gdula-Argasińska J, Muszyńska B, Tyszka-Czochara M, Librowski T, Opoka W (2015) Metal responsive transcription factor 1 (MTF-1) regulates zinc dependent cellular processes at the molecular level. Acta Biochim Pol 62(3):491–498. https://doi.org/10.18388/abp.2015_1038

    Article  CAS  PubMed  Google Scholar 

  55. Kim JH, Jeon J, Shin M, Won Y, Lee M, Kwak JS, Lee G, Rhee J, Ryu JH, Chun CH, Chun JS (2014) Regulation of the catabolic cascade in osteoarthritis by the zinc-ZIP8-MTF1 axis. Cell 156(4):730–743. https://doi.org/10.1016/j.cell.2014.01.007

    Article  CAS  PubMed  Google Scholar 

  56. Cao XN, Yan C, Liu DY, Peng JP, Chen JJ, Zhou Y, Long CL, He DW, Lin T, Shen LJ, Wei GH (2015) Fine particulate matter leads to reproductive impairment in male rats by overexpressing phosphatidylinositol 3-kinase (PI3K)/protein kinase B (Akt) signaling pathway. Toxicol Lett 237(3):181–190. https://doi.org/10.1016/j.toxlet.2015.06.015

    Article  CAS  PubMed  Google Scholar 

  57. Bryan HK, Olayanju A, Goldring CE, Park BK (2013) The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochem Pharmacol 85(6):705–717. https://doi.org/10.1016/j.bcp.2012.11.016

    Article  CAS  PubMed  Google Scholar 

  58. Qin S, Hou DX (2016) Multiple regulations of Keap1/Nrf2 system by dietary phytochemicals. Mol Nutr Food Res 60(8):1731–1755. https://doi.org/10.1002/mnfr.201501017

    Article  CAS  PubMed  Google Scholar 

  59. Li D, Ni S, Miao KS, Zhuang C (2019) PI3K/Akt and caspase pathways mediate oxidative stress-induced chondrocyte apoptosis. Cell Stress Chaperones 24(1):195–202. https://doi.org/10.1007/s12192-018-0956-4

    Article  CAS  PubMed  Google Scholar 

  60. Zhang X, Liang D, Chi ZH, Chu Q, Zhao C, Ma RZ, Zhao Y, Li H (2015) Effect of zinc on high glucose-induced epithelial-to-mesenchymal transition in renal tubular epithelial cells. Int J Mol Med 35(6):1747–1754. https://doi.org/10.3892/ijmm.2015.2170

    Article  CAS  PubMed  Google Scholar 

  61. Jin X, Jia T, Liu R, Xu S (2018) The antagonistic effect of selenium on cadmium-induced apoptosis via PPAR-γ/PI3K/Akt pathway in chicken pancreas. J Hazard Mater 357:355–362. https://doi.org/10.1016/j.jhazmat.2018.06.003

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was supported by Hebei Natural Science Foundation (grant no. H2021314001 and H2022314001) and S&T Program of Hebei (grant no. 226Z7722G).

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Authors and Affiliations

  1. Graduate School of Hebei Medical University, Shijiazhuang, 050017, China

    Junsheng Liu

  2. Department of College of Chemistry and Materials Science, Hebei Normal University, Shijiazhuang, 050024, China

    Xin Zuo, Yuanjing Li & Shusong Wang

  3. Graduate School of Chengde Medical University, Chengde, 067000, China

    Jiajie Bi & Shusong Wang

  4. Hebei Key Laboratory of Reproductive Medicine, Hebei Reproductive Health Hospital, Shijiazhuang, 050071, China

    Huanhuan Li, Jing Ma & Shusong Wang

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  1. Junsheng Liu
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Contributions

Junsheng Liu, Xin Zuo, Jiajie Bi, Huanhuan Li, Yuanjing Li collected the samples and performed the experiments. Xin Zuo and Jing Ma analyzed the data and wrote the manuscript. Jing Ma and Shusong Wang conceived the idea, designed the study, collected the funds, and revised the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Shusong Wang.

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All experimental procedures were approved by the Ethics Committee of Hebei Provincial Reproductive Health Hospital (animal ethics approval no. 2021-003), with every effort made to minimize both the number of animals used and their suffering.

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Liu, J., Zuo, X., Bi, J. et al. Palliative Effect of Combined Application of Zinc and Selenium on Reproductive Injury Induced by Tripterygium Glycosides in Male Rats. Biol Trace Elem Res (2024). https://doi.org/10.1007/s12011-023-04054-8

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